Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Stoichiometric control of organic carbon–nitrate relationships from soils to the sea

Abstract

The production of artificial fertilizers, fossil fuel use and leguminous agriculture worldwide has increased the amount of reactive nitrogen in the natural environment by an order of magnitude since the Industrial Revolution1. This reorganization of the nitrogen cycle has led to an increase in food production2, but increasingly causes a number of environmental problems1,3. One such problem is the accumulation of nitrate in both freshwater and coastal marine ecosystems. Here we establish that ecosystem nitrate accrual exhibits consistent and negative nonlinear correlations with organic carbon availability along a hydrologic continuum from soils, through freshwater systems and coastal margins, to the open ocean. The trend also prevails in ecosystems subject to substantial human alteration. Across this diversity of environments, we find evidence that resource stoichiometry (organic carbon:nitrate) strongly influences nitrate accumulation by regulating a suite of microbial processes that couple dissolved organic carbon and nitrate cycling. With the help of a meta-analysis we show that heterotrophic microbes maintain low nitrate concentrations when organic carbon:nitrate ratios match the stoichiometric demands of microbial anabolism. When resource ratios drop below the minimum carbon:nitrogen ratio of microbial biomass4, however, the onset of carbon limitation appears to drive rapid nitrate accrual, which may then be further enhanced by nitrification. At low organic carbon:nitrate ratios, denitrification appears to constrain the extent of nitrate accretion, once organic carbon and nitrate availability approach the 1:1 stoichiometry5 of this catabolic process. Collectively, these microbial processes express themselves on local to global scales by restricting the threshold ratios underlying nitrate accrual to a constrained stoichiometric window. Our findings indicate that ecological stoichiometry can help explain the fate of nitrate across disparate environments and in the face of human disturbance.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: NO3- concentration as a function of DOC or POC concentration among Earth’s major ecosystems.
Figure 2: Resource stoichiometry controls on microbial NO3- processing.

References

  1. 1

    Galloway, J. N. et al. Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320, 889–892 (2008)

    ADS  CAS  Article  Google Scholar 

  2. 2

    Smil, V. Nitrogen in crop production: an account of global flows. Glob. Biogeochem. Cycles 13, 647–662 (1999)

    ADS  CAS  Article  Google Scholar 

  3. 3

    Vitousek, P. M., Mooney, H. A., Lubchenco, J. & Melillo, J. M. Human domination of Earth’s ecosystems. Science 277, 494–499 (1997)

    CAS  Article  Google Scholar 

  4. 4

    Sterner, R. W. & Elser, J. J. Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere (Princeton University Press, 2002)

    Google Scholar 

  5. 5

    Richards, F. A. in Chemical Oceanography (eds Riley, J. P. & Skirrow, G.) Vol. 1, 611–645 (Academic Press, 1965)

    Google Scholar 

  6. 6

    Vitousek, P. M. & Howarth, R. W. Nitrogen limitation on land and sea: how can it occur. Biogeochemistry 13, 87–115 (1991)

    Article  Google Scholar 

  7. 7

    Mulholland, P. J. et al. Stream denitrification across biomes and its response to anthropogenic nitrate loading. Nature 452, 202–205 (2008)

    ADS  CAS  Article  Google Scholar 

  8. 8

    Barnes, R. T. & Raymond, P. A. Land use controls on the delivery, processing, and removal of nitrogen from small watersheds: insights from the dual isotopic composition of stream nitrate. Ecol. Appl 10.1890/08-1328 (in the press)

  9. 9

    Arango, C. P. & Tank, J. L. Land use influences the spatiotemporal controls in nitrification and denitrification in headwater streams. J. N. Am. Benthol. Soc. 27, 90–107 (2008)

    Article  Google Scholar 

  10. 10

    Bohlke, J. K. et al. Multi-scale measurements and modeling of denitrification in streams with varying flow and nitrate concentration in the upper Mississippi River basin, USA. Biogeochemistry 93, 117–141 (2009)

    CAS  Article  Google Scholar 

  11. 11

    Hungate, B. A., Dukes, J. S., Shaw, M. R., Luo, Y. Q. & Field, C. B. Nitrogen and climate change. Science 302, 1512–1513 (2003)

    CAS  Article  Google Scholar 

  12. 12

    Manzoni, S., Trofymow, J. A., Jackson, R. B. & Porporato, A. Stoichiometric controls on carbon, nitrogen, and phosphorus dynamics in decomposing litter. Ecol. Monogr. 80, 89–106 (2010)

    Article  Google Scholar 

  13. 13

    Hill, A. R., Devito, K. J., Campagnolo, S. & Sanmugdas, K. Subsurface denitrification in a forest riparian zone: interactions between hydrology and supplies of nitrate and organic carbon. Biogeochemistry 51, 193–223 (2000)

    Article  Google Scholar 

  14. 14

    Hedin, L. O. et al. Thermodynamic constraints on nitrogen transformations and other biogeochemical processes at soil-stream interfaces. Ecology 79, 684–703 (1998)

    Google Scholar 

  15. 15

    Goodale, C. L., Aber, J. D., Vitousek, P. M. & McDowell, W. H. Long-term decreases in stream nitrate: successional causes unlikely; possible links to DOC? Ecosystems 8, 334–337 (2005)

    CAS  Article  Google Scholar 

  16. 16

    Evans, C. D. et al. Evidence that soil carbon pool determines susceptibility of semi-natural ecosystems to elevated nitrogen leaching. Ecosystems 9, 453–462 (2006)

    CAS  Article  Google Scholar 

  17. 17

    Monteith, D. T. et al. Dissolved organic carbon trends resulting from changes in atmospheric deposition chemistry. Nature 450, 537–540 (2007)

    ADS  CAS  Article  Google Scholar 

  18. 18

    Sarmiento, J. L. & Gruber, N. Ocean Biogeochemical Dynamics (Princeton University Press, 2006)

    Book  Google Scholar 

  19. 19

    McGroddy, M. E., Daufresne, T. & Hedin, L. O. Scaling of C:N:P stoichiometry in forests worldwide: implications of terrestrial Redfield-type ratios. Ecology 85, 2390–2401 (2004)

    Article  Google Scholar 

  20. 20

    Cleveland, C. C. & Liptzin, D. C:N:P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85, 235–252 (2007)

    Article  Google Scholar 

  21. 21

    Anderson, T. R., Hessen, D. O., Elser, J. J., & Urabe, J. Metabolic stoichiometry and the fate of excess carbon and nutrients in consumers. Am. Nat. 165, 1–15 (2005)

    Article  Google Scholar 

  22. 22

    Apple, J. K. & del Giorgio, P. A. Organic substrate quality as the link between bacterioplankton carbon demand and growth efficiency in a temperate salt-marsh estuary. Multidisc. J. Microb. Ecol. 1, 729–742 (2007)

    CAS  Google Scholar 

  23. 23

    Jahnke, R. A. & Craven, D. B. Quantifying the role of hetertrophic bacteria in the carbon cycle: A need for respiration rate measurements. Limnol. Oceanogr. 40, 436–441 (1995)

    ADS  CAS  Article  Google Scholar 

  24. 24

    del Giorgio, P. A. & Cole, J. J. Bacterial growth efficiency in natural aquatic systems. Annu. Rev. Ecol. Syst. 29, 503–541 (1998)

    Article  Google Scholar 

  25. 25

    Tezuka, Y. Bacterial regeneration of ammonium and phosphate as affected by the carbon: nitrogen: phosphorus ratio of organic substrates. Microb. Ecol. 19, 227–238 (1990)

    CAS  Article  Google Scholar 

  26. 26

    Mulholland, M. R. & Lomas, M. W. in Nitrogen In The Marine Environment (eds Capone, D. et al.) 303–361 (Academic Press, 2008)

    Book  Google Scholar 

  27. 27

    Perakis, S. S. & Hedin, L. O. Nitrogen loss from unpolluted South American forests mainly via dissolved organic compounds. Nature 415, 416–419 (2002)

    ADS  Article  Google Scholar 

  28. 28

    Raymond, P. A. & Bauer, J. E. Use of 14C and 13C natural abundances for evaluating riverine, estuarine, and coastal DOC and POC sources and cycling: a review and synthesis. Org. Geochem. 32, 469–485 (2001)

    CAS  Article  Google Scholar 

  29. 29

    Cebrian, J. Patterns in the fate of production in plant communities. Am. Nat. 154, 449–468 (1999)

    Article  Google Scholar 

  30. 30

    Allen, A. P. & Gillooly, J. F. Towards an integration of ecological stoichiometry and the metabolic theory of ecology to better understand nutrient cycling. Ecol. Lett. 12, 369–384 (2009)

    Article  Google Scholar 

Download references

Acknowledgements

We thank N. Fierer, D. McKnight, J. Neff, W. Wieder and P. Vitousek for their contributions to the ideas and text reflected here, and R. Cory and R. Jaffe for unpublished data. We also thank all the organizations, institutions, collaborative projects and scientists that provided unpublished data via online repositories, without which this analysis would be impossible. We are particularly grateful for the contributions made by scientists affiliated with the US LTER network and the JGOFS/BCO-DMO; see a detailed list of data sets, associated Principal Investigators and access information in the Supplementary Information Notes.

Author Contributions P.G.T. conceived the project, gathered the requisite data, and performed statistical analyses. P.G.T and A.R.T. developed the conceptual model, interpreted the empirical findings, and wrote the manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Philip G. Taylor.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Figures S1-S6 with legends, a Supplementary Discussion, Supplementary Tables S1-S6 and Supplementary References and Data Lists. (PDF 3104 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Taylor, P., Townsend, A. Stoichiometric control of organic carbon–nitrate relationships from soils to the sea. Nature 464, 1178–1181 (2010). https://doi.org/10.1038/nature08985

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing